What is known about the care and support provided for an ageing population with lived experience of chronic viral hepatitis as they near end‐of‐life: A scoping review

Abstract Ageing with a chronic hepatitis B (HBV) or hepatitis C (HCV) infection is an emerging public health priority. For people living with chronic viral hepatitis, their disease progression into old age is both underpinned by their existing blood borne virus and the potential emergence of other infectious and non‐infectious conditions. These twinned pathways bring additional challenges to the care and support for people as they near end of life. This scoping review sought to examine what is known about the experiences of the end‐of‐life phase of an increasing population ageing with HBV and HCV in studies conducted in high‐income settings and published in peer reviewed literature (2010–2021). In interpreting this literature, we found that challenges in determining the end‐of life phase for people with lived experience of HBV or HCV are exacerbated by the conflation of aetiologies into a singular diagnosis of end‐stage liver disease. Studies overwhelmingly reported the clinical aspects of end‐of‐life care (i.e. prognosis assessment and symptom management) with less attention paid to educative aspects (i.e. advance care directives and surrogate decision makers, discussion of treatment options and determining goals of care). Psychosocial interventions (i.e. quality of life beyond symptom management, including emotional/spiritual support and family and bereavement support) received limited attention in the literature, though there was some recognition that psychosocial interventions should be part of end‐of‐life care provision. Given the focus on the prominent disease presentation of liver cirrhosis and/or end‐stage liver disease, the social and cultural dimensions of these infections have received less attention in the literature on end‐of‐life in the context of chronic viral hepatitis.


| INTRODUC TI ON
Ageing with a chronic hepatitis B (HBV) or hepatitis C (HCV) infection is an emerging public health priority as people living with these inflections represent a range of specialised health needs among Australia's rapidly ageing population. In particular, the increasing life expectancy of these affected populations warrants specific attention to the effects of co-morbidities and poly-pharmacies that may contribute to or compound ageing as they near end of life (Card et al., 2020;Heron et al., 2019;Siefried et al., 2018). At the same time, behavioural, social and structural factors may impede equity in health outcomes at this life phase (Mao et al., 2019). While HBV and HCV are distinct diseases and should not be conflated in clinical contexts, people with lived experience of HBV or HCV can be united by their chronic condition, long asymptomatic periods of infection, long-term effects on the liver and the stigma associated with the diseases. Accordingly, we sought to determine how end-of-life care and support is provided for an increasing population of people ageing with chronic HBV and/or HCV; that is, the care given to people who have stopped treatment to cure or control their disease as they are considered to be at the end of their life course (which can include physical, emotional, social and spiritual support for patients and their families). Limited existing research and the pressing need for stronger evidence for this ageing population warrants the examination of HBV and HCV concurrently.

| Background
In 2016, the World Health Organization drew worldwide attention to the issue of viral hepatitis with the publication of its inaugural global health strategy that set ambitious targets for the elimination of viral hepatitis as a major public health threat by 2030 (World Health Organization, 2016). Effective vaccination, improved treatment and cure (in the case of HCV) mean that living and dying in older age with lived experience of HCV or HBV is now possible-and probable-for many (El-Serag & Kramer, 2008;Wong et al., 2020).
As such, people who live with the effects of chronic HBV or HCV represent an emerging subset of an ageing population. While experiences of ageing are challenging for all (The Academy of Medical Sciences, 2018;Meagher et al., 2019), people living with chronic HBV or HCV represent a distinct population associated with higher rates of age-related co-morbidities and other specific care needs (Mao et al., 2019;Richmond & Wallace, 2014;Ridruejo & Silva, 2012).
Outside of clinical or physical symptomatology, older people living in marginalised social circumstances also experience fewer opportunities for end-of-life support due to social or economic deprivation, stigmatisation, and/or poor health (Ellis et al., 2016;Hughes & Cartwright, 2015). Yet, little research exists that addresses the intersection of ageing, chronic illness and end-of-life care in the context of chronic viral hepatitis and the small number of studies that have done so have concentrated on specific groups that reflects their different needs, such people who inject drugs, migrant communities and people experiencing homelessness (McNeil & Guirguis-Younger, 2012;Sumalinog et al., 2017;Taylor et al., 2006).
Globally, it is estimated that approximately 296 million people were chronically infected with HBV in 2019 (World Health Organization, 2021). Only 30.4 million people (10.5% of all people estimated to be living with HBV) were aware of their infection and less than a quarter (22%) of the people diagnosed were on treatment in 2019 (World Health Organization, 2021). The absolute number of infected individuals continues to grow in line with the global population, with 1.5 million new infections each year (World Health Organization, 2021). Clinical management, including regular monitoring and pharmaceutical treatment effectively reduces the risk of mortality resulting from the infection (Lok & McMahon, 2009).
Additionally, the introduction of neonatal vaccination programs has considerably reduced the incidence and prevalence of HBV infection in several areas of high endemicity, and in Australia, where the authorship team are based, the Australian National Immunisation Program now provides HBV vaccination at birth and during infancy.
While the 95% overall National Strategy target for infant HBV immunisation was reached in 2020, it is estimated that 27% of the people living with HBV in Australia remain undiagnosed (MacLachlan What is known about this topic?
• Increasing commitment to the global elimination of viral hepatitis has meant that people are now ageing with lived experience of hepatitis B and/or hepatitis C.
• People living with chronic hepatitis B and/or hepatitis C represent a distinct population associated with higher rates of age-related co-morbidities and other specific care needs.
• There is currently little research existing that addresses the intersection of ageing, chronic illness and end-of-life care in the context of chronic viral hepatitis.

What does this paper add to this topic?
• Synthesising insights into determining the end-of-life phase for people with lived experience of hepatitis B and/or hepatitis C, as well as their care and support needs at this stage of life, confirms the limited range of evidence available.
• Critical to interpreting this evidence is the question of how viral hepatitis is understood in relation to the endof-life phase given the focus on the prominent disease presentation of liver cirrhosis and/or end-stage liver disease.
• An emphasis on clinical and educative aspects of end-oflife care meant that psychosocial dimensions received less attention in the literature, and the social and cultural dimensions of ageing and dying with hepatitis B and/or hepatitis C were obscured. et al., 2020). Of the estimated 222,559 people in Australia living with HBV in 2020, the majority (61%) of them were born overseas (MacLachlan et al., 2020), therefore incidence cannot be prevented through local vaccination initiatives alone. As a result, the prevalence of HBV-related disease among the Australian population is estimated to increase in the future.
An estimated 71 million people are living with chronic HCV infections around the world (World Health Organization, 2021), including an estimated 199,230 Australians (Kirby Institute, 2018). While WHO estimates that 290,000 people died from HCV-related causes in 2019 (World Health Organization, 2021), new data also show that 9.4 million people are receiving treatment for chronic infections-a nearly 10-fold increase from 2015 (World Health Organization, 2021). Unlike HBV, HCV treatments affording the possibility of cure have been available for several decades. Until recently, however, the only option has been interferon-based therapy, a notoriously long and arduous regime with limited success rates (Hellard et al., 2009). The treatment landscape was dramatically reconfigured with the advent of new direct-acting antivirals (DAAs) in 2014. Described as 'one of the great advances in clinical medicine in recent decades' (Dore & Hajarizadeh, 2018, p. 269), DAAs offer simpler, shorter adherence regimens, markedly reduced side effects and cure rates of near 100% (Banerjee & Reddy, 2016;Dore & Feld, 2015). Yet, the absence of an HCV vaccine means that behavioural interventions (such as the use of sterile injecting equipment) remain the chief form of prevention for both primary infections and reinfections.
Limited empirical evidence exists for the effectiveness of HCV treatment-as-prevention (i.e. treatment as a tool for limiting the spread of an infection in epidemics in a particular setting; see Hajarizadeh et al., 2016). In Australia, early trials show a significant reduction in HCV incidence for people who inject drugs in carceral settings (Hajarizadeh et al., 2021), but scaleup outside of these settings has been limited to date. Improving rates of testing and diagnosis are also crucial, with only 15.2 million out of the estimated 71 million people living with HCV worldwide aware of their serostatus (World Health Organization, 2021). Due to the slow progression of the virus, the more severe consequences of HCV typically manifest 30 years post infection. Low testing rates and the often-asymptomatic nature of acute infections mean that people can live for years with undetected infection and the possibility of developing long-term liver damage before diagnosis and treatment (World Health Organization, 2021). As a result, people who were infected with HCV in their 20s are now at heightened risk of liver damage by the time they reach their 50s (Shepard et al., 2005). Moreover, despite the clear benefits of DAA therapy through HCV infection cure, potential longer-term clinical implications are less known (Alavi et al., 2019). While successful courses of DAA treatments among HCV-affected people have resulted in lower mortality among younger populations, ongoing risk of liverrelated diseases are still present among older populations, especially for those where there is a lengthy delay between infection and treatment.
What constitutes 'end of life' in the context of ageing for these cohorts is difficult to determine. On the one hand, there is a lack of clarity around accelerated ageing linked to hepatitis-related morbidities, given differences between symptomatolgy, iatrogenic effects and other comorbidities. On the other hand, an individual's hepatitis status-and their care and support needs related to that infectioncan be obscured by other more prominent disease profiles as people near the end of life. Moreover, there is a need to understand whether age is an appropriate proxy for 'severity of liver disease' (Richmond & Wallace, 2014) or whether there are specific age-related issues associated with HBV and HCV outside of that disease. Generally, end-of-life detertminations and palliative care clinical referrals are based on disease progressions that have definitive markers (e.g. a quick or a prolonged, but overall consistent, decline of physical function and quality of life where treatment options are no longer life sustaining) (Amblàs-Novellas et al., 2016;Lunney et al., 2003). HBV and HCV viral infection may indeed confound this determination, given the curative potential of treatment and/or liver transplant.
Moreover, while the benefits of timely referral to palliative care are well-established in other disease contexts (Friedman et al., 2002;Hui et al., 2018;Temel et al., 2010), people with end-stage liver disease experience low rates of referral to specialist palliative care, and those who are referred are often delayed or very late Low et al., 2018;Peng et al., 2019;Sumalinog et al., 2017;Valery et al., 2015). Collectively, these factors highlight considerable challenges in meeting the supportive and end-of-life care needs in the context of ageing with HBV and HCV.

| ME THODS
A scoping review methodology was determined to be the most appropriate method for responding to the research question: how is end-of-life care and support provided for an increasing cohort of people ageing with lived experience of HBV and HCV? (See Table 1).
A scoping review provides a transparent, rigorous and structured process for exploring the literature in order to map the breadth of existing research-and to identify knowledge and research gaps-on a specific topic of interest, especially where there is limited published research (Arksey & O'Malley, 2005). Unlike narrative reviews, scoping reviews require 'analytical reinterpretation' of the published study findings, which is valuable for assessing the contribution of the research that is available (Levac et al., 2010). Compared to systematic reviews, scoping reviews do not focus on evaluating the methodological quality of the studies being appraised, which means there is greater flexibility in looking across a diverse range of study types (Arksey & O'Malley, 2005).
This review scoped peer-reviewed academic literature published in English from 1 January 2010 to 12 January 2021. This date range was selected to reflect the significant changes in the relevant fields of viral hepatitis, palliative and/or end-of-life care; that is, to capture changes following the introduction of DAAs for HCV infection alongside palliative medicine becoming established as an area of speciality. Relevant literature was identified by searching key databases with consistent search parameters and using EndNote as a data management tool (see Table 1 for a list of databases and search parameters and Figure 1 for a chart of the selection process).
Keywords aimed to capture all intersecting research concerning the disease profile (HBV, HCV and their comorbidities and mortalities), Stage 4-charting the data All included references were charted in Excel where relevant information was synthesised and interpreted by sifting, charting and sorting according to key issues and themes. A 'descriptive-analytical' method was used, which involves applying an analytical framework to the literature and collating information on each. The list of included references were exported into the 'data charting form', and a coding framework developed to characterise key features of each.
Stage 5-reporting the results All results were collated to provide an overview of the material reviewed, categorised into themes that responded to the following questions: 1. How is end of life determined in the context of ageing with lived experience of chronic viral hepatitis? 2. How is care and support at end-of-life provided for people with lived experience of chronic viral hepatitis?

Stage 6-consultation exercise
Informal consultations took place with three expert key informants from relevant organisations or with relevant expertise across July and September 2021. phase of life (ageing, dying and end-of-life) and treatment type (palliative and supportive care, advance care planning and other non-clinical and non-curative care). Editorials, letters to the editor, reviews, and/or commentaries with no original research were excluded, as were publications where their main content was clinical protocols or practitioner guidelines, or articles on palliative care not in the context of the target population. Articles that explored experiences of liver cirrhosis associated with HBV or HCV where findings also referenced palliative care and/or advance care planning in both acute and non-acute settings were included.

F I G U R E 1 Flowchart of selection process
At each stage in the overall process, screening was undertaken independently by at least two of the authors, and any disparities over inclusion or exclusion were resolved by a further independent screening by another author until consensus was reached.

| RE SULTS
The search strategy generated 1094 unique citations of which 23 articles met the inclusion criteria (see Table 2). The majority of arti- noted that the non-stratification of disease aetiology in their mortality prediction was a limitation of their study (see also Hansen, Leo, et al., 2015). Given the overall lack of differentiation over how ageing and associated morbidities intersect with clinical markers that might indicate the need for end-of-life care, we organised our analysis into two broad domains that responded to the research sub-questions posed, the relevance of which was confirmed by consultations with experts. These two domains explore the challenges in distinguishing both the end-of-life phase and the care that is provided at this point in an individual's life course. How the end-of-life phase was determined (see Table 2 Of those discharged to hospice, this cohort were older in age, more likely to have ascites and prior infections requiring high volumes of paracentesis, and less likely to be listed for liver transplantation.

|
Grade 3-4 hepatic encephalopathy was also found to be the greatest predictor of discharge to hospice. However, the authors noted that low MELD scores (models for stratifying the severity of end-stage liver disease for transplant planning) were associated with patients discharged to home, which may not adequately capture debilitating hepatic encephalopathy and/or refractory ascites, leaving them to suffer in what they called 'MELD purgatory' where low scores do not reflect patients' symptom burden (p2575). Finally, Fukui et al. (2017) reviewed hospitalised Medicare beneficiaries (United States; aged over 65 years or those with qualified health conditions) with chronic liver disease discharged to hospice over a 4-year period (n = 2179) to determine the costs related to the underutilisation of hospice (as compared to a control of beneficiaries without chronic liver disease).
Despite overall consistent yearly increases in discharge to hospice, patients with chronic liver disease had higher rates of hospice death, hospital mortality, and 1-year mortality compared to those without chronic liver disease. The authors attribute these patterns to higher rates of, and more aggressive, life-prolonging therapies, in which late referrals to hospice were unlikely to be optimally beneficial.
In interpreting this literature, we found that challenges in ascer-

| Challenges in ascertaining the range of end-of-life care in the context of ageing with chronic viral hepatitis
It is important to interpret findings relating to how support is iden- , or as a separate or specialty service available in specialist palliative care referrals (Low et al., 2017;Najafian et al., 2019;Patel et al., 2020;Sprange et al., 2020;Valery et al., 2017;Wang et al., 2021). Other articles discussed disease treatment more broadly (Hansen, Rosenkranz, et al., 2015), symptom management outside of palliative specialities (Hansen et al., 2014;Hansen, Leo, et al., 2015) and emotional and other support needs (Gray-Renfrew et al., 2020;Valery et al., 2017) outside of palliative specialities.
Studies overwhelmingly reported the clinical aspects of endof-life care (i.e. prognosis assessment and symptom management).
Intervention studies introduced early (Baumann et al., 2015;Shinall et al., 2019) and structured (Lamba et al., 2012) palliative care consultations into standard liver transplantation and inpatient hepatology services, in effect bundling palliative care with ongoing clinical assessment and care. All studies found clear benefits in the concurrent provision of palliative and curative care, documenting improvements in symptomatology, including depressive symptoms (Baumann et al., 2015), and decreases in length of hospital stay (Lamba et al., 2012;Shinall et al., 2019), and increases in withdrawal of life-support interventions (Lamba et al., 2012) compared to those patients not receiving the intervention. Importantly, the need for effective clinical management is supported by measurements of physical and psychological distress in patients, where higher rates of symptomatology among people living with HCV compared with other aetiologies of end-stage liver disease were found, specifically fatigue (Hansen, Leo, et al., 2015) and pain burden (Hansen et al., 2014). Rather than treating for presence of pain, Hansen and colleagues (2015) recommend that clinical management include attention to shifts in frequency, severity and distress levels at different points in patients' disease course. Reporting on the same study within a different article, Hansen et al. (2014) also draw attention to the intersection of pain with other symptoms, such as fatigue, and how patients manage pain symptoms on their own, such as napping and reducing activity levels, as well as seeking professional help and taking pain medication, which point to other measures of support outside of clinical interventions. In addition, the authors found that 30%-40% of their sample reported no pain medication use despite reporting moderate pain, but they also noted that clinical pain management differs between those on and those declined/delisted for liver transplantation waiting lists (e.g. strong opioid vs. weak medication). Another study similarly reported that despite support accessed by patients diagnosed with cirrhosis in a liver clinic that included a range of allied health services, such as dieticians, pharmacists, psychologists/psychiatrists, spiritual support and social workers, there was less use of those allied support services compared to use of services related to acute symptomatology (Valery et al., 2017). Finally, while patients' acute medical care is well-coordinated, there was less attention to ongoing care in the community .
There was mixed evidence in terms of outcomes related to educa- about emotional support and support to cease alcohol and substance use as they were about clinical symptom management and disease management (Valery et al., 2017). Indeed, negative emotional responses to advanced liver disease were equally evident in a secondary analysis of a longitudinal study, with Gray-Renfrew et al. (2020) describing fear, anger, guilt and shame, with causal factors associated with these emotional responses, including shock of diagnosis, uncertainty around declining health and pessimism over lack of cure, which point to the need for further psychosocial support. Uncertainty was a dominant theme in perspectives of patients recruited from inpatient hepatology wards, evident in patients' confusion between symptoms associated with the disease and those related to chronological ageing, confusion over the term 'cirrhosis' and its relation to liver disease, and the unpredictable trajectory of the illness following diagnosis . Uncertainty was also evident in how the disease impacts everyday life, with limited awareness of psychosocial support services available, which was further hampered by a perceived lack of communication, information and education from healthcare professionals.
Further, in another study of patients with advanced hepatocellular carcinoma at the end of life (Hansen, Rosenkranz, et al., 2015), uncertainty intersected with illness perception and decision to start and nav-   (Podymow et al., 2006). This focus presents challenges in teasing out other experiences of dying in the context of ageing that may be relevant to people with lived experience of HBV or HCV. This scoping review also underscores that palliative care research does not focus on specific conditions, for example, a blood-borne virus, but rather focusses on outcomes, such as symptom management.
Although scoping reviews do not evaluate the methodological HCV was overwhelmingly represented in the studies under review, and in some cases, HBV was specifically excluded from studies (Fukui et al., 2017) or combined with HCV as 'viral hepatitis' (Brown et al., 2016;Sprange et al., 2020). care and support needs, there are additional opportunities to consider not only the relationship between palliative care and oncology, but other relationships between other disciplines and specialities because of the intersecting multimorbidity that may be present.
Indeed, any emphasis on oncology in understanding end-of-life needs for this cohort may be a limitation as not all people living with chronic viral hepatitis and liver disease die of liver cancer as a direct cause. These challenges are further compounded when the uneven trajectory of viral hepatitis is considered. Patients once considered within the end-of-life phase may need to be effectively 're-phased' following treatment or transplantation. As such, policy approaches to palliative and end-of-life care need to consider the 'spectrum and unpredictability' of underlying disease (Mazzarelli et al., 2018).
Given the focus on the prominent disease presentation (i.e. liver cirrhosis, end-stage or advanced liver disease) the social and cultural dimensions of these infections have received less attention. While not covered in detail in the literature, stigma and discrimination are key factors in patient experiences as they near end of life, which present significant concerns around health equity. Indeed, the number of proxies to describe identities and lifestyles associated with hepatitis (injecting drug use, sex between men and so on) should remain a concern for policy makers and clinicians alike. Moreover, stigma plays a critical role in influencing people's decision-making around disclosure and treatment seeking in both infections (Freeland et al., 2022;Jin et al., 2020;Treloar & Rhodes, 2009), which has implications for clinical management. Stigma and discrimination related to hepatitis serostatus has also been found to pervade all aspects of an individual life (Freeland et al., 2022), suggesting that its effects radiate across the whole life course. The social implications of living with a stigmatised disease, then, not only influence diagnosis, disclosure and treatment decisions, but inevitably those associated with the end-of-life. Specialist palliative care providers, as well as generalist clinicians and oncologists, should consider additional care and support needs that relate to the psychosocial elements of end-of-life. An emphasis on the provision of clinician-led information (i.e. by general practitioners or liver specialists) may hinder the provision of more comprehensive information, especially those pertaining to psycho-social needs, required by patients. Previous studies on HBV have shown that most patients will obtain relevant information pertaining to their experience of the disease from their clinician, not through other potentially culturally resonant sources (Hopwood, 2013). Cultural understandings of life and death need to be acknowledged, which in turn could inform how information is framed and relayed. Indeed, the focus of the scoped articles lies in the structured and biomedical response to end-of-life, rather than any care and support that can take place outside clinical settings, which can impede our understanding of the needs of people with HBV given their cultural and linguistic diversity on Australia. Finally, care in the community remains an important consideration for endof-life support. A person-centred care could benefit from a consideration of the unique experiences of people with lived experience of HBV and HCV where ageing and dying lies on a continuum, rather than a single transition point.

AUTH O R S ' CO NTR I B UTI O N S
The initial idea for a scoping review on the topic came from Kerryn Drysdale, Jake Rance, Limin Mao and Carla Treloar.

FU N D I N G I N FO R M ATI O N
This scoping review was funded by the Australian Department of Health. The contributions of the investigator team were supported by the Centre for Social Research in Health, which receives some funding from a range of external agencies.

CO N FLI C T O F I NTE R E S T
The authors declare that there is no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing not applicable to this article as no datasets were generated or analysed during the current study.